Abstract: How does the brain orchestrate perceptions, thoughts and actions from the spiking activity of its neurons? Previous single neuron recording research has regarded spike pattern variability as noise that should be averaged out to reveal the brain’s representation of invariant input. An alternatively view is that variability of spikes is centrally coordinated and that this brain-generated ensemble pattern in cortical structures is a potential source of cognition. Large-scale recordings from neuronal ensembles now offer opportunities for challenging and testing these competing theoretical frames. A postulated signature of the cell assembly is that its participants show a higher probability of spiking together than with members of other assemblies, even in the absence of external inputs. Interactions among parallel-recorded hippocampal neurons revealed a consistent temporal structure beyond that predicted from the environmental inputs. We find that prediction of spike times of hippocampal pyramidal neurons is improved using the spike times of simultaneously recorded neurons, over prediction from the animal’s trajectory in space, or a spatially-dependent theta phase modulation. Thus, we suggest that the assembly organization arises from the internal dynamics of neuronal circuits. Assemblies are organized most efficiently within 10-30ms, suggesting that cell assemblies are synchronized at this timescale (gamma cycles). Seven to nine cell assemblies form assembly sequences within a theta cycle. The most active assemble occupies the trough of theta representing “here and now”, flanked by representation of past and future places on the descending and ascending phase of theta, respectively. The “lifetime” of an assembly in the dorsal hippocampus is 1-2 sec, corresponding to 7 to 14 cycles of theta. The lifetime of oscillating assemblies is internally regulated and can be accelerated by the locomotion speed of the rat and possible other gain factors. The internally generated assemblies can give rise to a perpetually changing composition of assembly membership even in the absence of environmental or idiothetic inputs. We hypothesize that the mechanisms underlying the intrinsically shifting assembly sequences is the substrate of episodic memory.
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